Introduction

The world's forests are disappearing at a rate of 130,000 square kilometers per year [1]. One of the major centers of deforestation is the Amazon Basin, an area that encompasses portions of Brazil, Bolivia, Peru, Ecuador, Colombia, Venezuela, Guyana, Suriname, and French Guiana (Fig. 1). The Amazon is the world's largest rain forest, with approximately 50% of its area (4,100,000 square kilometers) located in Brazil [2]. Intensive deforestation of the Brazilian Amazon began in the 1970s, and 70% of the clearing can be attributed to medium-sized and large cattle ranches [3, 4]. Additional clearing for soybean agriculture [4] and selective logging practices [5, 6] have further reduced the amount of intact forest. Activity is primarily concentrated in the “arc of deforestation,” located in the southern and eastern areas of the Brazilian Amazon [3], but new highway development plans [4] and colonization projects [7, 8] threaten to increase deforestation across the Amazon.

Fig. 1.

The Amazon Basin in South America is comprised of areas of Brazil, Bolivia, Peru, Ecuador, Colombia, Venezuela, Guyana, Suriname, and French Guiana. Approximately 4,100,000 square kilometers (50%) of the forested area is located in Brazil

One of the consequences of deforestation is forest fragmentation, an ever-increasing global phenomenon affecting the persistence of healthy forest ecosystems across the planet [9]. Forest fragmentation occurs when sections of contiguous forest are cleared, thereby leaving a mosaic of patches surrounded by a non-forested matrix. As deforestation for agriculture or urban development continues, the remaining forest becomes increasingly patchy, affecting local climate [10, 11], species richness and distribution [10, 12, 13], predator-prey interactions [14], seed dispersal [15, 16], and habitat suitability [17, 18].

Although there is a body of literature examining the effects of forest fragmentation on fauna, flora, climate, and ecological processes, to date there is no consensus as to which factors are primarily responsible for influencing a species' response to forest fragmentation [1920–21]. Furthermore, data are lacking for many taxa. For example, in the primate literature the majority of the behavioral ecology research in disturbed habitats focuses on a handful of species, such as howler monkeys (genus Alouatta) [16, 22, 23]. Thus, conclusions regarding how primates are affected by habitat fragmentation may not be applicable to underrepresented species in the literature due to differences in the species' behavior and ecology.

Current human practices throughout the tropics threaten the future research and understanding of little-studied taxa, as well as the species' conservation. In this article I illustrate how recent development plans in the Brazilian Amazon may affect the conservation of the nonhuman primates in the region both directly (i.e., deforestation, hunting) and indirectly (i.e., loss of scientific knowledge).

Overview of Conservation Issue

Deforestation of the Brazilian Amazon forest for cattle ranches and soybean cultivation has been coupled with intense development of the transportation infrastructure. As roads are paved and more roads are built, areas that were once remote become easily accessible to humans. Often such developments result in an increase in logging and deforestation [6, 2425–26], as well as hunting [18, 27]. In the Brazilian Amazon, two highways, the BR-163 (Santarém-Cuiabá) and BR-319 (Manaus-Porto Velho), are of particular concern [26, 28].

The region surrounding a third highway, BR-174 (Manaus-Boa Vista), which leads to Venezuela (Fig. 2), is the focal area for a controversial plan by the Brazilian federal agency Superintenděncia da Zona Franca de Manaus (SUFRAMA). The plan calls for at least six colonization projects that would bring 180 families into an area alongside the BR-174, as well as feeder roads such as ZF-3 [7, 8]. The colonization sites would be located approximately 80 km north of Manaus, a large city of approximately 1.6 million inhabitants [29]. Such a project would threaten federally protected areas, a portion of the planned Central Amazonia Conservation Corridor, important research sites operated by the Instituto Nacional da Pesquisas de Amazǒnia (INPA) and Large Scale Biosphere-Atmosphere Experiment in Amazonia (LBA), and the existence of the Biological Dynamics of Forest Fragments Project (BDFFP), the longest-running study on forest fragmentation [7].

Fig. 2.

Deforestation along the BR-174. Landsat ETM+ satellite imagery from 2006 shows the pattern of deforestation along, and spreading outward from, the BR-174 highway. The BR-174 extends north from Manaus to Venezuela, passing through the BDFFP study area. Dark green areas are forested, light green areas are secondary growth, and pink areas are non-forested

The BDFFP, operated by INPA and the Smithsonian Tropical Research Institute, began in 1979 and has resulted in approximately 600 publications, books, dissertations, and theses by Brazilian and foreign scientists and students on the consequences of forest fragmentation [7]. Gascon and Bierregaard, Jr. [30] and Gascon et al. [31] provide a history of the project and a review of the research findings. The study site (Fig. 3), occupies an area of 1,000 square kilometers, and is in the midst of the area slated by SUFRAMA for the colonization projects, even though sections of the BDFFP study area are national protected areas [7, 8]. Already there has been an influx of human inhabitants to the study area (Fig. 4), and BDFFP has suffered from theft, intentional fires, hunting, and logging [7]. Six primate species reside in the BDFFP study area: red howler monkey (Alouatta seniculus), black spider monkey (Ateles paniscus), brown capuchin monkey (Cebus apella), brown bearded saki (Chiropotes satanas chiropotes)¹, white-faced saki monkey (Pithecia pithecia), and golden-handed tamarin (Saguinus midas). Although research at BDFFP has been ongoing since 1979, primate research in the forest fragments has been sporadic, with in-depth behavioral and ecological research only on red howler monkeys [3536373839–40], white-faced saki monkeys [4142–43], and bearded saki monkeys [44]. Therefore, there is still much to learn regarding the responses of the primates to forest fragmentation.

Fig. 3.

The Biological Dynamics of Forest Fragments Project (BDFFP) is located approximately 80 km north of Manaus, the capital of the state of Amazonas. Forest fragments are located throughout three cattle ranches, or fazendas, Dimona, Porto Alegre, and Esteio. Cabo Frio and Km 41 are two continuous forest sites. Fragments are black, clear-cut areas and secondary forest areas are white, and old growth forest is gray. The SUFRAMA colonization plan would settle families within the area of BDFFP

Discussion

SUFRAMA's colonization plan to bring in 180 families to the area has raised serious concern by scientists who foresee the plan having negative ecological, economical, and sociological consequences [7, 8]. Agricultural projects in the Amazon are often not profitable [4], due to the area's low soil fertility. Ranchers near the BDFFP's forest fragments have experienced this firsthand [45]. In fact, one of the main uses of forest in central Amazonia is burning it for charcoal (W. Laurance, pers. comm.). Therefore there is concern that the colonists would not benefit from the colonization plan [8], and there would be increased rates of hunting, logging, and charcoal production. In addition, it is important to note that the plots of land in the SUFRAMA settlement areas would be sold to landowners, some for the purpose of weekend leisure; thus, the settlers are not currently homeless (R. Luizão, pers. comm.).

The possible demise of the BDFFP, a research site that spans three decades, would be a great scientific and educational loss. Approximately three decades of research have been conducted at the BDFFP, yet the BDFFP has also been a source of employment and educational opportunities (e.g., training in science and management) for local residents, for Brazilians from other areas of the country, and for the international community [7, 46]. Past and present BDFFP researchers have also partnered with other agencies to work with the rural population on agroforestry projects (e.g., education, training, distribution of native seedlings), and to provide educational materials on how to make a living without disturbing the protected areas (R. Luizão, pers. comm.). Scientists also credit the cooperation between the local landowners and the BDFFP researchers for the success of the BDFFP project [45]. Therefore, increased human colonization of the study area threatens all aspects of the BDFFP, including the conservation of the primates in the area.

Fig. 4.

Settlers within the Biological Dynamics of Forest Fragments Project (BDFFP) study area have illegally cut native forest. Theft, hunting, and intentional fires have also posed problems to the BDFFP. This photograph depicts one settlement in July 2007. Photo courtesy of BDFFP/Carlos da Costa.

The BDFFP is a unique and valuable resource for the study of primates and forest fragmentation. First, censuses of the primates occurred prior to the isolation of the forest fragments, and subsequent censuses of the forest fragments have been intermittently conducted throughout the past three decades [474849–50]. These data are imperative to determine the current status of the resident primate populations, to document any patterns of primate immigrations and extinctions that have arisen during the past 30 years, and to relate the presence or absence of the species to predictive variables (e.g., fragment size, distance to continuous forest, and condition of the matrix). Second, the variations in fragment size (1–100 ha) and the configurations of fragments within the surrounding matrix (which varies from pasture to tall secondary growth forest) allow researchers to study the species within the fragments, as well as their use, or avoidance, of the surrounding landscape. Third, the primates at BDFFP represent six species that vary in body size, diet, home range size, and social structure. Therefore, comparisons of the responses of the species to fragments of various sizes and surrounded by various compositional matrices, are unique opportunities.

The findings to-date have shed light on the variability in responses of the six resident primate species to forest fragmentation (Table 1). Differences between species were apparent upon the initial isolation of the BDFFP forest fragments [47]. Furthermore, since the 1980s, some species (e.g., red howler monkey) have persisted in the various forest fragments, while other species (e.g., black spider monkey, Fig. 5) have remained absent from the majority of the forest fragments [474849–50]. Understanding why some species are re-colonizing the forest fragments decades later, and how their use of the fragments' resources differs from that of animals living in continuous forest, is critical for the conservation planning of the species.

Table 1

Primate Presence 2003–2006. The presence of the six primate species is noted for the three size classes of forest fragments: 100 ha, 10 ha, and 1 ha. For each size class, the proportion of fragments in which each species was present is noted. (*) indicates that the species was present in the forest fragment for less than 20 percent of the study.

Implications for Conservation

Overall there is a lack of knowledge of the Amazon's fauna and flora [51], including the behavioral ecology of many free-ranging primates [52]. If the SUFRAMA colonization plan is put into effect, it could disturb several major scientific research sites in the area, as well as the Central Amazonian Conservation Corridor. More importantly, an increase in colonists could result in the local demise of many plant and animal species, including many of the primates.

Primates are readily hunted in many parts of the tropics, and an influx of settlers to an area would likely bring extra hunting pressure. Human colonization in the eastern Brazilian Amazon has greatly affected the mammal community [53]. All six primate species inhabiting the BDFFP region are hunted in some areas of the Amazon, though hunting pressure varies [5455565758–59].

To preserve biodiversity in areas experiencing human disturbance, it is important to understand how habitat modifications alter species survival over time. For example, primate presence has fluctuated at the BDFFP, thereby creating opportunities to study species that were not present in the forest fragments during the 1980s. Therefore, the continuation of primate research (e.g., censuses, behavioral studies, land cover classifications) at BDFFP is critical to understanding how (and to what extent) the primates use the forest fragments and the surrounding matrix. Unfortunately, the colonization of the area by 180 families, and the subsequent increased human pressure on vulnerable species, is cause for alarm.

Fig. 5.

Red Howler monkeys (Alouatta seniculus) are more prevalent in forest fragments than the other five primate species at BDFFP. They are commonly found in fragments as small as 10 ha, and intermittently reside in fragments as small as 1 ha. Black spider monkeys (Ateles paniscus) have been the least prevalent primate species in the forest fragments at BDFFP. These large-bodied frugivores often face intense hunting pressure throughout the Amazon. Photos by Sarah Boyle.

There is serious conservation concern for the future of the BDFFP primates, in particular those that are virtually absent from the majority of the forest fragments (i.e., black spider monkeys, brown capuchin monkeys), those that appear to be severely isolated from other groups due to their hesitance to cross a young matrix (i.e., bearded saki monkeys), and those that may be currently under hunting pressure in the immediate areas surrounding the BDFFP reserves (i.e., black spider monkeys, red howler monkeys, and brown capuchin monkeys).

There is hope. Researchers and environmental advocates have partnered with like-minded Brazilian agencies to urge SUFRAMA to halt the colonization plans; to release the findings of its 2004 land-use report, which was developed by both SUFRAMA and scientists; and to consult with scientific and research management organizations and government agencies, as well as the public, prior to commencing any forest-colonization plans [7, 8, 60]. As a result of increased media attention regarding the colonization plan, both in Brazil and abroad [7, 8, 606162–63], SUFRAMA has temporarily suspended activities related to forest settlement near the BDFFP area (R. Luizão, pers. comm.). Furthermore, reports Luizão, the BDFFP has been invited to submit proposals for funding to develop a formal management plan for both the BDFFP and other regional protected areas. It is crucial that such collaboration and progress continue, due to the importance of the forest that is at risk by the SUFRAMA colonization plan.